Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Abiotic stress responses in plants

Abstract

Plants cannot move, so they must endure abiotic stresses such as drought, salinity and extreme temperatures. These stressors greatly limit the distribution of plants, alter their growth and development, and reduce crop productivity. Recent progress in our understanding of the molecular mechanisms underlying the responses of plants to abiotic stresses emphasizes their multilevel nature; multiple processes are involved, including sensing, signalling, transcription, transcript processing, translation and post-translational protein modifications. This improved knowledge can be used to boost crop productivity and agricultural sustainability through genetic, chemical and microbial approaches.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Abiotic stress can be sensed in various cellular compartments to initiate molecular responses at multiple levels.
Fig. 2: Proposed salinity and drought stress sensing and signalling mechanisms.
Fig. 3: Proposed cold and heat stress sensing and signalling mechanisms.
Fig. 4: Stress responses at the levels of transcription and transcript processing.
Fig. 5: Stress responses at the levels of translation and epigenetic regulation.
Fig. 6: Genetic–chemical–microbial strategy for improving abiotic stress resistance in crops.

Similar content being viewed by others

References

  1. Bailey-Serres, J., Parker, J. E., Ainsworth, E. A., Oldroyd, G. E. D. & Schroeder, J. I. Genetic strategies for improving crop yields. Nature 575, 109–118 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Zhang, H., Zhao, Y. & Zhu, J. K. Thriving under stress: how plants balance growth and the stress response. Dev. Cell 55, 529–543 (2020).

    CAS  PubMed  Google Scholar 

  3. Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016). This Review proposes the concept of dispersed stress sensing in various cell parts.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Chen, X. X. et al. Protein kinases in plant responses to drought, salt, and cold stress. J. Integr. Plant Biol. 63, 53–78 (2021).

    CAS  PubMed  Google Scholar 

  5. Gupta, A., Rico-Medina, A. & Cano-Delgado, A. I. The physiology of plant responses to drought. Science 368, 266–269 (2020).

    CAS  PubMed  Google Scholar 

  6. Takahashi, F., Kuromori, T., Urano, K., Yamaguchi-Shinozaki, K. & Shinozaki, K. Drought stress responses and resistance in plants: from cellular responses to long-distance intercellular communication. Front. Plant Sci. 11, 556972 (2020).

    PubMed  PubMed Central  Google Scholar 

  7. Yang, Y. & Guo, Y. Unraveling salt stress signaling in plants. J. Integr. Plant Biol. 60, 796–804 (2018).

    CAS  PubMed  Google Scholar 

  8. Zhang, J. Y., Li, X. M., Lin, H. X. & Chong, K. Crop improvement through temperature resilience. Annu. Rev. Plant Biol. 70, 753–780 (2019).

    CAS  PubMed  Google Scholar 

  9. Yuan, F. et al. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014).

    CAS  PubMed  Google Scholar 

  10. Jojoa-Cruz, S. et al. Cryo-EM structure of the mechanically activated ion channel OSCA1.2. eLife 7, e41845 (2018).

    PubMed  PubMed Central  Google Scholar 

  11. Liu, X., Wang, J. & Sun, L. Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2. Nat. Commun. 9, 5060 (2018).

    PubMed  PubMed Central  Google Scholar 

  12. Maity, K. et al. Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating. Proc. Natl Acad. Sci. USA 116, 14309–14318 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Hamilton, E. S. et al. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350, 438–441 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Hamilton, E. S. & Haswell, E. S. The tension-sensitive ion transport activity of MSL8 is critical for its function in pollen hydration and germination. Plant Cell Physiol. 58, 1222–1237 (2017).

    CAS  PubMed  Google Scholar 

  15. Jiang, Z. et al. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572, 341–346 (2019). This work demonstrates an important role for MOCA1-dependent GIPC production in plant response to high salinity.

    CAS  PubMed  Google Scholar 

  16. Rennie, E. A. et al. Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis. Plant Cell 26, 3314–3325 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Laohavisit, A. et al. Salinity-induced calcium signaling and root adaptation in arabidopsis require the calcium regulatory protein annexin1. Plant Physiol. 163, 253–262 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Ma, L. et al. The SOS2–SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev. Cell 48, 697–709.e5 (2019).

    CAS  PubMed  Google Scholar 

  19. Feng, W. et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28, 666–675.e5 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhao, C. et al. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc. Natl Acad. Sci. USA 115, 13123–13128 (2018). Together with Feng et al. (2018), this work supports the critical roles of the LRX–RALF–FER regulatory module in salt sensing and salt tolerance.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Sangwan, V., Orvar, B. L., Beyerly, J., Hirt, H. & Dhindsa, R. S. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 31, 629–638 (2002).

    CAS  PubMed  Google Scholar 

  22. Cui, Y. et al. Cyclic nucleotide-gated ion channels 14 and 16 promote tolerance to heat and chilling in rice. Plant Physiol. 183, 1794–1808 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Liu, Q. et al. The calcium transporter ANNEXIN1 mediates cold-induced calcium signaling and freezing tolerance in plants. EMBO J. 7, e104559 (2020). This study reports cold-induced Ca2+ influx through the Ca2+ transporter AtANN1.

    Google Scholar 

  24. Ma, Y. et al. COLD1 confers chilling tolerance in rice. Cell 160, 1209–1221 (2015).

    CAS  PubMed  Google Scholar 

  25. Wang, J. et al. Transcriptional activation and phosphorylation of OsCNGC9 confer enhanced chilling tolerance in rice. Mol. Plant 14, 315–329 (2020).

    PubMed  Google Scholar 

  26. Jiang, B. et al. Cold-Induced CBF–pif3 interaction enhances freezing tolerance by stabilizing the phyB thermosensor in Arabidopsis. Mol. Plant 13, 894–906 (2020).

    CAS  PubMed  Google Scholar 

  27. Jung, J. H. et al. Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889 (2016).

    CAS  PubMed  Google Scholar 

  28. Legris, M. et al. Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900 (2016).

    CAS  PubMed  Google Scholar 

  29. Casal, J. J. & Balasubramanian, S. Thermomorphogenesis. Annu. Rev. Plant Biol. 70, 321–346 (2019).

    CAS  PubMed  Google Scholar 

  30. Jung, J. H. et al. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 585, 256–260 (2020). This study identifies a thermosensor protein that displays a direct biophysical (that is, phase transition) response to increasing temperature.

    CAS  PubMed  Google Scholar 

  31. Scharf, K. D., Berberich, T., Ebersberger, I. & Nover, L. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 1819, 104–119 (2012).

    CAS  PubMed  Google Scholar 

  32. Kumar, S. V. & Wigge, P. A. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136–147 (2010).

    CAS  PubMed  Google Scholar 

  33. McAinsh, M. R. & Pittman, J. K. Shaping the calcium signature. N. Phytol. 181, 275–294 (2009).

    CAS  Google Scholar 

  34. Marti, M. C., Stancombe, M. A. & Webb, A. A. R. Cell- and stimulus type-specific intracellular free Ca2+ signals in arabidopsis. Plant Physiol. 163, 625–634 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Hrabak, E. M. et al. The Arabidopsis CDPK–SnRK superfamily of protein kinases. Plant Physiol. 132, 666–680 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Tang, R. J., Wang, C., Li, K. & Luan, S. The CBL–CIPK calcium signaling network: unified paradigm from 20 years of discoveries. Trends Plant Sci. 25, 604–617 (2020).

    CAS  PubMed  Google Scholar 

  37. Tang, R. J. et al. Tonoplast CBL–CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc. Natl Acad. Sci. USA 112, 3134–3139 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Kim, Y., Park, S., Gilmour, S. J. & Thomashow, M. F. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 75, 364–376 (2013).

    CAS  PubMed  Google Scholar 

  39. Geiger, D. et al. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase–phosphatase pair. Proc. Natl Acad. Sci. USA 106, 21425–21430 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Klingler, J. P., Batelli, G. & Zhu, J. K. ABA receptors: the START of a new paradigm in phytohormone signalling. J. Exp. Bot. 61, 3199–3210 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Min, M. K. et al. Two clade A phosphatase 2Cs expressed in guard cells physically interact with abscisic acid signaling components to induce stomatal closure in rice. Rice 12, 37 (2019).

    PubMed  PubMed Central  Google Scholar 

  42. Sirichandra, C. et al. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 583, 2982–2986 (2009).

    CAS  PubMed  Google Scholar 

  43. Sun, S. J. et al. Protein kinase OsSAPK8 functions as an essential activator of S-type anion channel OsSLAC1, which is nitrate-selective in rice. Planta 243, 489–500 (2016).

    CAS  PubMed  Google Scholar 

  44. Wang, P. et al. Mapping proteome-wide targets of protein kinases in plant stress responses. Proc. Natl Acad. Sci. USA 117, 3270–3280 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Wu, Q. Q. et al. ZmOST1 mediates abscisic acid regulation of guard cell ion channels and drought stress responses. J. Integr. Plant Biol. 61, 478–491 (2019).

    CAS  PubMed  Google Scholar 

  46. Ma, Y. et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064–1068 (2009).

    CAS  PubMed  Google Scholar 

  47. Park, S. Y. et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Chen, K. et al. Abscisic acid dynamics, signaling, and functions in plants. J. Integr. Plant Biol. 62, 25–54 (2020).

    CAS  PubMed  Google Scholar 

  49. Ding, Y. et al. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in arabidopsis. Dev. Cell 32, 278–289 (2015). This study demonstrates ABA-independent activation of SnRK2.6/OST1 by cold stress.

    CAS  PubMed  Google Scholar 

  50. Katsuta, S. et al. Arabidopsis Raf-like kinases act as positive regulators of subclass III SnRK2 in osmostress signaling. Plant J. 103, 634–644 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Lin, Z. et al. A RAF–SnRK2 kinase cascade mediates early osmotic stress signaling in higher plants. Nat. Commun. 11, 613 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Soma, F., Takahashi, F., Suzuki, T., Shinozaki, K. & Yamaguchi-Shinozaki, K. Plant Raf-like kinases regulate the mRNA population upstream of ABA-unresponsive SnRK2 kinases under drought stress. Nat. Commun. 11, 1373 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Takahashi, Y. et al. MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat. Commun. 11, 12 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Fabregas, N., Yoshida, T. & Fernie, A. R. Role of Raf-like kinases in SnRK2 activation and osmotic stress response in plants. Nat. Commun. 11, 6184 (2020). Together with Lin et al. (2020), Soma at al. (2020) and Takahashi et al. (Nature Communications, 2020), this paper demonstrates that hyperosmotic stress rapidly activates RAFs, leading to phosphorylation and activation of ABA-independent SnRK2s.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Lin, Z. et al. Initiation and amplification of SnRK2 activation in abscisic acid signaling. Nat. Commun. 12, 2456 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Gobert, A., Isayenkov, S., Voelker, C., Czempinski, K. & Maathuis, F. J. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc. Natl Acad. Sci. USA 104, 10726–10731 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Isner, J. C., Begum, A., Nuehse, T., Hetherington, A. M. & Maathuis, F. J. M. KIN7 kinase regulates the vacuolar TPK1 K+ channel during stomatal closure. Curr. Biol. 28, 466–472 e4 (2018).

    CAS  PubMed  Google Scholar 

  58. Chen, X. X. et al. Arabidopsis U-box E3 ubiquitin ligase PUB11 negatively regulates drought tolerance by degrading the receptor-like protein kinases LRR1 and KIN7. J. Integr. Plant Biol. 63, 494–509 (2021).

    CAS  PubMed  Google Scholar 

  59. Yang, T. et al. Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal. Behav. 5, 991–994 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhao, C. et al. MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev. Cell 43, 618–629 e5 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Danquah, A. et al. Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J. 82, 232–244 (2015).

    CAS  PubMed  Google Scholar 

  62. de Zelicourt, A., Colcombet, J. & Hirt, H. The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci. 21, 677–685 (2016).

    PubMed  Google Scholar 

  63. Qi, J. et al. Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J. Integr. Plant Biol. 60, 805–826 (2018).

    CAS  PubMed  Google Scholar 

  64. Chan, K. X., Phua, S. Y., Crisp, P., McQuinn, R. & Pogson, B. J. Learning the languages of the chloroplast: retrograde signaling and beyond. Annu. Rev. Plant Biol. 67, 25–53 (2016).

    CAS  PubMed  Google Scholar 

  65. Pesaresi, P. & Kim, C. Current understanding of GUN1: a key mediator involved in biogenic retrograde signaling. Plant Cell Rep. 38, 819–823 (2019).

    CAS  PubMed  Google Scholar 

  66. Hua, D. P. et al. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24, 2546–2561 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Wu, F. H. et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581 (2020).

    CAS  PubMed  Google Scholar 

  68. Brandt, B. et al. Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4, e03599 (2015).

    PubMed Central  Google Scholar 

  69. Geiger, D. et al. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc. Natl Acad. Sci. USA 107, 8023–8028 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Meinhard, M., Rodriguez, P. L. & Grill, E. The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214, 775–782 (2002).

    CAS  PubMed  Google Scholar 

  71. Miller, G. et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45 (2009).

    PubMed  Google Scholar 

  72. Suzuki, N. et al. Temporal–spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25, 3553–3569 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Choi, W. G. et al. Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J. 90, 698–707 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Choi, W. G., Toyota, M., Kim, S. H., Hilleary, R. & Gilroy, S. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc. Natl Acad. Sci. USA 111, 6497–6502 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Zandalinas, S. I., Fichman, Y. & Mittler, R. Vascular bundles mediate systemic reactive oxygen signaling during light stress. Plant Cell 32, 3425–3435 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Fichman, Y., Myers, R. J., Grant, D. G. & Mittler, R. Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis. Sci. Signal. 14, eabf0322 (2021).

    CAS  PubMed  Google Scholar 

  77. Zandalinas, S. I. & Mittler, R. Vascular and non-vascular transmission of systemic reactive oxygen signals during wounding and heat stress. Plant Physiol. 186, 1721–1733 (2021).

    CAS  PubMed  Google Scholar 

  78. Takahashi, F. et al. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556, 235–238 (2018). This work demonstrates small peptide-mediated root to shoot signalling in response to drought.

    CAS  PubMed  Google Scholar 

  79. Dinneny, J. R. Developmental responses to water and salinity in root systems. Annu. Rev. Cell Dev. Biol. 35, 239–257 (2019).

    CAS  PubMed  Google Scholar 

  80. Leftley, N., Banda, J., Pandey, B., Bennett, M. & Voss, U. Uncovering how auxin optimizes root systems architecture in response to environmental stresses. Cold Spring Harb. Perspect. Biol. https://doi.org/10.1101/cshperspect.a040014 (2021).

    Article  PubMed  Google Scholar 

  81. Hua, J. From freezing to scorching, transcriptional responses to temperature variations in plants. Curr. Opin. Plant Biol. 12, 568–573 (2009).

    CAS  PubMed  Google Scholar 

  82. Jacob, P., Hirt, H. & Bendahmane, A. The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol. J. 15, 405–414 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Ma, S. & Bohnert, H. J. Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol. 8, R49 (2007). This study in A. thaliana summarizes common transcriptional responses to various environmental stresses.

    PubMed  PubMed Central  Google Scholar 

  84. Zhu, J. K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Narusaka, Y. et al. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 34, 137–148 (2003).

    CAS  PubMed  Google Scholar 

  86. Yamaguchi-Shinozaki, K. & Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781–803 (2006).

    CAS  PubMed  Google Scholar 

  87. Liu, Q. et al. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Stockinger, E. J., Gilmour, S. J. & Thomashow, M. F. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl Acad. Sci. USA 94, 1035–1040 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Shinwari, Z. K. et al. An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250, 161–170 (1998).

    CAS  PubMed  Google Scholar 

  90. Haake, V. et al. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol. 130, 639–648 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Nakashima, K. et al. Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol. Biol. 42, 657–665 (2000).

    CAS  PubMed  Google Scholar 

  92. Fowler, S. & Thomashow, M. F. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14, 1675–1690 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Kreps, J. A. et al. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129–2141 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Seki, M. et al. Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct. Integr.Genomics 2, 282–291 (2002).

    CAS  PubMed  Google Scholar 

  95. Chinnusamy, V., Zhu, J. & Zhu, J. K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444–451 (2007).

    CAS  PubMed  Google Scholar 

  96. Tang, K. et al. The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes. J. Integr. Plant Biol. 62, 258–263 (2020).

    CAS  PubMed  Google Scholar 

  97. Thomashow, M. F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571–599 (1999).

    CAS  PubMed  Google Scholar 

  98. Medina, J., Catalá, R. & Salinas, J. The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci. 180, 3–11 (2011).

    CAS  PubMed  Google Scholar 

  99. Santiago, J. et al. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 60, 575–588 (2009).

    CAS  PubMed  Google Scholar 

  100. Szostkiewicz, I. et al. Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J. 61, 25–35 (2010).

    CAS  PubMed  Google Scholar 

  101. Claeys, H., Van Landeghem, S., Dubois, M., Maleux, K. & Inze, D. What is stress? Dose–response effects in commonly used in vitro stress assays. Plant Physiol. 165, 519–527 (2014). This report highlights that plant abiotic stress responses are strongly dependent on the stress levels.

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Watkinson, J. I. et al. Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol. 133, 1702–1716 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Hugouvieux, V., Kwak, J. M. & Schroeder, J. I. An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106, 477–487 (2001).

    CAS  PubMed  Google Scholar 

  104. Okamoto, M. et al. Sm-like protein-mediated RNA metabolism is required for heat stress tolerance in arabidopsis. Front. Plant Sci. 7, 1079 (2016).

    PubMed  PubMed Central  Google Scholar 

  105. Wu, S. J., Wang, L. C., Yeh, C. H., Lu, C. A. & Wu, S. J. Isolation and characterization of the Arabidopsis heat-intolerant 2 (hit2) mutant reveal the essential role of the nuclear export receptor EXPORTIN1A (XPO1A) in plant heat tolerance. N. Phytol. 186, 833–842 (2010).

    CAS  Google Scholar 

  106. Zhan, X. et al. An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and ABA responses. Nat. Commun. 6, 8139 (2015).

    CAS  PubMed  Google Scholar 

  107. Gong, Z. et al. RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc. Natl Acad. Sci. USA 99, 11507–11512 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Guan, Q. et al. A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25, 342–356 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Lu, C. A. et al. DEAD-Box RNA helicase 42 plays a critical role in pre-mRNA splicing under cold stress. Plant Physiol. 182, 255–271 (2020).

    CAS  PubMed  Google Scholar 

  110. Wang, B. et al. The DEAD-box RNA helicase SHI2 functions in repression of salt-inducible genes and regulation of cold-inducible gene splicing. J. Exp. Bot. 71, 1598–1613 (2020).

    CAS  PubMed  Google Scholar 

  111. Ling, Y. et al. Pre-mRNA splicing repression triggers abiotic stress signaling in plants. Plant J. 89, 291–309 (2017).

    CAS  PubMed  Google Scholar 

  112. Marquez, Y., Brown, J. W., Simpson, C., Barta, A. & Kalyna, M. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res. 22, 1184–1195 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Ding, F. et al. Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genomics 15, 431 (2014).

    PubMed  PubMed Central  Google Scholar 

  114. Li, Y. et al. Comprehensive profiling of alternative splicing landscape during cold acclimation in tea plant. BMC Genomics 21, 65 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Wang, Z. J. et al. ABA signalling is fine-tuned by antagonistic HAB1 variants. Nat. Commun. 6, 8138 (2015).

    PubMed  Google Scholar 

  116. Gu, J. et al. Spliceosomal protein U1A is involved in alternative splicing and salt stress tolerance in Arabidopsis thaliana. Nucleic Acids Res. 46, 1777–1792 (2018).

    CAS  PubMed  Google Scholar 

  117. Chong, G. L., Foo, M. H., Lin, W. D., Wong, M. M. & Verslues, P. E. Highly ABA-induced 1 (HAI1)-interacting protein HIN1 and drought acclimation-enhanced splicing efficiency at intron retention sites. Proc. Natl Acad. Sci. USA 116, 22376–22385 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Chakrabarti, M., de Lorenzo, L., Abdel-Ghany, S. E., Reddy, A. S. N. & Hunt, A. G. Wide-ranging transcriptome remodelling mediated by alternative polyadenylation in response to abiotic stresses in Sorghum. Plant J. 102, 916–930 (2020).

    CAS  PubMed  Google Scholar 

  119. Tellez-Robledo, B. et al. The polyadenylation factor FIP1 is important for plant development and root responses to abiotic stresses. Plant J. 99, 1203–1219 (2019).

    CAS  PubMed  Google Scholar 

  120. Ye, C. T., Zhou, Q., Wu, X. H., Ji, G. L. & Li, Q. S. Q. Genome-wide alternative polyadenylation dynamics in response to biotic and abiotic stresses in rice. Ecotoxicol. Environ. Saf. 183, 109485 (2019).

    CAS  PubMed  Google Scholar 

  121. Rogers, K. & Chen, X. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25, 2383–2399 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Sunkar, R., Chinnusamy, V., Zhu, J. & Zhu, J. K. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12, 301–309 (2007).

    CAS  PubMed  Google Scholar 

  123. Sunkar, R., Kapoor, A. & Zhu, J. K. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18, 2051–2065 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Liu, Y. et al. MiR319 mediated salt tolerance by ethylene. Plant Biotechnol. J. 17, 2370–2383 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Zhou, M. et al. Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol. 161, 1375–1391 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Yang, C. H. et al. Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Env. 36, 2207–2218 (2013).

    CAS  Google Scholar 

  127. Merret, R. et al. Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana. Nucleic Acids Res. 43, 4121–4132 (2015). This work reveals that heat-induced ribosomal pausing in A. thaliana preferentially occurs on transcripts coding for HSC/HSP70 chaperone targets.

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Merret, R. et al. XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. Cell Rep. 5, 1279–1293 (2013).

    CAS  PubMed  Google Scholar 

  129. Nguyen, A. H. et al. Loss of Arabidopsis 5′–3′ exoribonuclease AtXRN4 function enhances heat stress tolerance of plants subjected to severe heat stress. Plant Cell Physiol. 56, 1762–1772 (2015).

    CAS  PubMed  Google Scholar 

  130. Merret, R. et al. Heat shock protein HSP101 affects the release of ribosomal protein mRNAs for recovery after heat shock. Plant Physiol. 174, 1216–1225 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Zhang, L. et al. Mutations in eIF5B confer thermosensitive and pleiotropic phenotypes via translation defects in Arabidopsis thaliana. Plant Cell 29, 1952–1969 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Yu, H. et al. STCH4/REIL2 confers cold stress tolerance in Arabidopsis by promoting rRNA processing and CBF protein translation. Cell Rep. 30, 229–242.e5 (2020).

    CAS  PubMed  Google Scholar 

  133. Wang, S. et al. Chloroplast RNA-binding protein RBD1 promotes chilling tolerance through 23S rRNA processing in Arabidopsis. PLoS Genet. 12, e1006027 (2016).

    PubMed  PubMed Central  Google Scholar 

  134. Ding, Y. et al. EGR2 phosphatase regulates OST1 kinase activity and freezing tolerance in Arabidopsis. EMBO J. 38, e99819 (2019). This study reports a mechanism for ABA-independent activation of SnRK2.6 in response to cold stress.

    PubMed  Google Scholar 

  135. Kilian, J. et al. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347–363 (2007).

    CAS  PubMed  Google Scholar 

  136. Willems, P. et al. The Plant PTM Viewer, a central resource for exploring plant protein modifications. Plant J. 99, 752–762 (2019).

    CAS  PubMed  Google Scholar 

  137. Feng, J., Chen, L. & Zuo, J. Protein S-nitrosylation in plants: current progresses and challenges. J. Integr. Plant Biol. 61, 1206–1223 (2019).

    PubMed  Google Scholar 

  138. Matamoros, M. A. & Becana, M. Molecular responses of legumes to abiotic stress: protein post-translational modifications and redox signaling. J. Exp. Bot. 72, 5876–5892 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Hu, J. et al. Nitric oxide regulates protein methylation during stress responses in plants. Mol. Cell 67, 702–710.e4 (2017).

    CAS  PubMed  Google Scholar 

  140. Zhang, H., Lang, Z. & Zhu, J. K. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489–506 (2018).

    CAS  PubMed  Google Scholar 

  141. Chang, Y. N. et al. Epigenetic regulation in plant abiotic stress responses. J. Integr. Plant Biol. 62, 563–580 (2020).

    CAS  PubMed  Google Scholar 

  142. Chinnusamy, V., Dalal, M. & Zhu, J. K. Epigenetic regulation of abiotic stress responses in plants. Plant Abiotic Stress https://doi.org/10.1002/9781118764374.ch8 (2014).

    Article  Google Scholar 

  143. Khan, A. R. et al. Vernalization treatment induces site-specific DNA hypermethylation at the VERNALIZATION-A1 (VRN-A1) locus in hexaploid winter wheat. BMC Plant Biol. 13, 209 (2013).

    PubMed  PubMed Central  Google Scholar 

  144. Xu, R. et al. Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis. J. Exp. Bot. 66, 5997–6008 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Yong-Villalobos, L. et al. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc. Natl Acad. Sci. USA 112, E7293–E7302 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Baek, D. et al. Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance. Plant Cell Physiol. 52, 149–161 (2011).

    CAS  PubMed  Google Scholar 

  147. Zheng, M. et al. Histone acetyltransferase GCN5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes. Plant J. 97, 587–602 (2019).

    CAS  PubMed  Google Scholar 

  148. Zhu, Y. et al. The arabidopsis nodulin homeobox factor AtNDX interacts with AtRING1A/B and negatively regulates abscisic acid signaling. Plant Cell 32, 703–721 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Zhang, B. et al. Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation. Proc. Natl Acad. Sci. USA 113, 12580–12585 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Zemach, A. et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Vaillant, I., Schubert, I., Tourmente, S. & Mathieu, O. MOM1 mediates DNA-methylation-independent silencing of repetitive sequences in Arabidopsis. EMBO Rep. 7, 1273–1278 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  152. Iwasaki, M. & Paszkowski, J. Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proc. Natl Acad. Sci. USA 111, 8547–8552 (2014). This study identifies MOM1 and DDM1 as two key factors that prevent transgenerational transmission of stress-induced epigenetic states.

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Jiang, C. et al. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 24, 1821–1829 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Lang-Mladek, C. et al. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol. Plant 3, 594–602 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Wibowo, A. et al. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife 5, e13546 (2016).

    PubMed  PubMed Central  Google Scholar 

  156. Sanchez, D. H. & Paszkowski, J. Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene. PLoS Genet. 10, e1004806 (2014).

    PubMed  PubMed Central  Google Scholar 

  157. Hirsch, C. N. et al. Insights into the maize pan-genome and pan-transcriptome. Plant Cell 26, 121–135 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Liu, Y. C. et al. Pan-genome of wild and cultivated soybeans. Cell 182, 162–176.e13 (2020).

    CAS  PubMed  Google Scholar 

  159. Qin, P. et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell 184, 3542–3558.e16 (2021).

    CAS  PubMed  Google Scholar 

  160. Munns, R. et al. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat. Biotechnol. 30, 360-U173 (2012).

    Google Scholar 

  161. Ren, Z. H. et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 37, 1141–1146 (2005).

    CAS  PubMed  Google Scholar 

  162. Zhang, M. et al. A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. N. Phytol. 217, 1161–1176 (2018).

    CAS  Google Scholar 

  163. Li, X. M. et al. Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat. Genet. 47, 827–833 (2015).

    CAS  PubMed  Google Scholar 

  164. Wang, Z. et al. Loss of salt tolerance during tomato domestication conferred by variation in a Na+/K+ transporter. EMBO J. 39, e103256 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  165. Wang, Z. et al. Natural variations in SlSOS1 contribute to the loss of salt tolerance during tomato domestication. Plant Biotechnol. J. 19, 20–22 (2021).

    CAS  PubMed  Google Scholar 

  166. Mao, H. D. et al. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat. Commun. 6, 8326 (2015).

    CAS  PubMed  Google Scholar 

  167. Wang, X. et al. Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat. Genet. 48, 1233–1241 (2016).

    CAS  PubMed  Google Scholar 

  168. Cui, M. et al. Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiol. Biochem. 49, 1384–1391 (2011).

    CAS  PubMed  Google Scholar 

  169. Mallikarjuna, G., Mallikarjuna, K., Reddy, M. K. & Kaul, T. Expression of OsDREB2A transcription factor confers enhanced dehydration and salt stress tolerance in rice (Oryza sativa L.). Biotechnol. Lett. 33, 1689–1697 (2011).

    CAS  PubMed  Google Scholar 

  170. Gupta, B. K. et al. Manipulation of glyoxalase pathway confers tolerance to multiple stresses in rice. Plant Cell Env. 41, 1186–1200 (2018).

    CAS  Google Scholar 

  171. Zhang, J. et al. Knockdown of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol. 176, 2082–2094 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  172. Waltz, E. Beating the heat. Nat. Biotechnol. 32, 610–613 (2014).

    CAS  PubMed  Google Scholar 

  173. Simmons, C. R. et al. Successes and insights of an industry biotech program to enhance maize agronomic traits. Plant Sci. 307, 110899 (2021).

    CAS  PubMed  Google Scholar 

  174. Lou, D., Wang, H. & Yu, D. The sucrose non-fermenting-1-related protein kinases SAPK1 and SAPK2 function collaboratively as positive regulators of salt stress tolerance in rice. BMC Plant Biol. 18, 203 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  175. Lu, Y. et al. Targeted, efficient sequence insertion and replacement in rice. Nat. Biotechnol. 38, 1402–1407 (2020). This paper reports a technology that allows highly efficient insertion of transcriptional or translational regulatory sequences in any gene of interest.

    CAS  PubMed  Google Scholar 

  176. Wang, M. G. et al. Optimizing base editors for improved efficiency and expanded editing scope in rice. Plant Biotechnol. J. 17, 1697–1699 (2019).

    PubMed  PubMed Central  Google Scholar 

  177. Zhan, X., Lu, Y., Zhu, J. K. & Botella, J. R. Genome editing for plant research and crop improvement. J. Integr. Plant Biol. 63, 3–33 (2020).

    Google Scholar 

  178. Zhu, H., Li, C. & Gao, C. Applications of CRISPR–Cas in agriculture and plant biotechnology. Nat. Rev. Mol. Cell Biol. 21, 661–677 (2020).

    CAS  PubMed  Google Scholar 

  179. Morran, S. et al. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol. J. 9, 230–249 (2011).

    CAS  PubMed  Google Scholar 

  180. Nakashima, K. et al. Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239, 47–60 (2014).

    CAS  PubMed  Google Scholar 

  181. Wang, P. C. et al. Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol. Cell 69, 100–112 (2018). This work elucidates an important mechanism underlying the antagonism between stress response and plant growth.

    CAS  PubMed  Google Scholar 

  182. Dobrenel, T. et al. TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67, 261–285 (2016).

    CAS  PubMed  Google Scholar 

  183. Cai, Z. Y. et al. GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 9651–9656 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  184. Li, J. F. et al. The GSK3-like kinase BIN2 is a molecular switch between the salt stress response and growth recovery in Arabidopsis thaliana. Dev. Cell 55, 367–380 (2020).

    CAS  PubMed  Google Scholar 

  185. Nolan, T. M., Vukasinovic, N., Liu, D. R., Russinova, E. & Yin, Y. H. Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32, 295–318 (2020).

    CAS  PubMed  Google Scholar 

  186. Srivastava, M. et al. SUMO conjugation to BZR1 enables brassinosteroid signaling to integrate environmental cues to shape plant growth. Curr. Biol. 30, 1410–1423 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  187. Wang, H. J. et al. Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol. Plant 11, 315–325 (2018).

    CAS  PubMed  Google Scholar 

  188. Cao, M. J. et al. An ABA-mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Res. 23, 1043–1054 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  189. Singh, R., Bhardwaj, V. K., Sharma, J. & Purohit, R. Identification of novel and selective agonists for ABA receptor PYL3. Plant Physiol. Biochem. 154, 387–395 (2020).

    CAS  PubMed  Google Scholar 

  190. Vaidya, A. S. et al. Dynamic control of plant water use using designed ABA receptor agonists. Science 366, eaaw8848 (2019).

    CAS  PubMed  Google Scholar 

  191. Cao, M. J. et al. Combining chemical and genetic approaches to increase drought resistance in plants. Nat. Commun. 8, 1183 (2017). This report demonstrates the power of combining genetic and chemical approaches for improving plant drought stress resistance.

    PubMed  PubMed Central  Google Scholar 

  192. Reinhold-Hurek, B., Bunger, W., Burbano, C. S., Sabale, M. & Hurek, T. Roots shaping their microbiome: global hotspots for microbial activity. Annu. Rev. Phytopathol. 53, 403–424 (2015).

    CAS  PubMed  Google Scholar 

  193. Vilchez, J. I. et al. DNA demethylases are required for myo-inositol-mediated mutualism between plants and beneficial rhizobacteria. Nat. Plants 6, 983–995 (2020).

    CAS  PubMed  Google Scholar 

  194. Liu, X. M. & Zhang, H. The effects of bacterial volatile emissions on plant abiotic stress tolerance. Front. Plant Sci. 6, 774 (2015).

    PubMed  PubMed Central  Google Scholar 

  195. Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009).

    CAS  PubMed  Google Scholar 

  196. Chen, K. et al. BONZAI proteins control global osmotic stress responses in plants. Curr. Biol. 30, 4815–4825.e4 (2020).

    CAS  PubMed  Google Scholar 

  197. Li, H. et al. MPK3-and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev. Cell 43, 630–642 (2017).

    CAS  PubMed  Google Scholar 

  198. Ding, Y. et al. OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J. 37, e98228 (2018).

    PubMed  PubMed Central  Google Scholar 

  199. Wang, X. et al. PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Dev. Cell 51, 222–235.e5 (2019).

    CAS  PubMed  Google Scholar 

  200. Liu, Z. et al. Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol. Cell 66, 117–128.e5 (2017).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors apologize to those colleagues whose work is not cited owing to space constraints. H.Z. and J-K.Z. have been supported by the Chinese Academy of Sciences. Z.G. acknowledges grants from the National Science Foundation of China (31730007, 32030008, 31921001).

Author information

Authors and Affiliations

Authors

Contributions

J.-K. Z. and H.Z. researched, discussed and wrote the article. All authors reviewed and/or edited the article before submission.

Corresponding authors

Correspondence to Huiming Zhang or Jian-Kang Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Genetics thanks F. Van Breusegem and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Hyperosmotic stress

Increased extracellular osmolarity that leads to cell dehydration.

Pectins

Acidic polysaccharides that are critical for plant cell wall properties such as cohesion and electrostatic potential.

Extensins

Hydroxyproline-rich glycoproteins that are essential components of the cell wall.

Phase transition

A qualitative change in the state of a system under a continuous change in an external parameter, such as the reversible condensation of certain proteins within cells in response to changing temperature.

Retrograde signalling

Signalling from organelles to the nucleus.

Systemic acquired acclimation

A systemic response to abiotic stimuli, which involves long-distance communication among cells belonging to different tissues or organs.

Epialleles

Isogenic alleles with different epigenetic modifications that are passed from generation to generation.

Quantitative trait loci

Chromosome regions that statistically contribute to the variability of a quantitative phenotype.

Genome-wide association studies

Approaches searching the entire genome using single-nucleotide polymorphisms for chromosome regions that show consistent correlation with a particular phenotype, within a large population of individuals with contrasting and varying degree of the phenotype.

Marker-assisted breeding

An approach for breeding in which the selection of desired individuals is based on the score of molecular markers.

Rhizosphere

The soil layer that surrounds, and is influenced by, plant roots.

Microbiota

All microorganisms that inhabit a defined region.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Zhu, J., Gong, Z. et al. Abiotic stress responses in plants. Nat Rev Genet 23, 104–119 (2022). https://doi.org/10.1038/s41576-021-00413-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41576-021-00413-0

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing